ISSN 1070–1524

Insect Predation of Seeds and Plant

Population Dynamics
Jianxin Zhang
Francis A. Drummond
Matt Liebman
and
Alden Hartke

Technical Bulletin 163 February 1997

MAINE AGRICULTURAL AND FOREST EXPERIMENT STATION

University of Maine
 Insect Predation of Seeds and
Plant Population Dynamics

Jianxin Zhang
Research Associate

Francis A. Drummond
Associate Professor

Matt Liebman
Associate Professor

and

Alden Hartke
Graduate Student

Department of Applied Ecology and Environmental Sciences

University of Maine
Orono, Maine 04469-5722
 ACKNOWLEDGMENTS
The authors wish to thank Dr. Eleanor Groden and Dr. Eric
Gallandt for critically reviewing the manuscript and Dr. Richard
Storch for editorial assistance. This work was funded by the United
States Department of Agriculture from a special CSRS research
grant for potato ecosystems.
 Contents

Introduction ...................................................................5
Predispersal Seed Predation .........................................5
Postdispersal Seed Predation ......................................10
Seed Predation And Plant Population Dynamics .......15
Plant Population Recruitment ...............................15
Seed Dispersal ........................................................17
Spatial Patterns of Plants ......................................17
Adaptation ..............................................................18
Plant Community Dynamics ..................................21
Weed Control With Seed Predators .............................22
References ....................................................................25
MAFES Technical Bulletin 163 5

INTRODUCTION
Seed production is a critical stage in the life history of plants.
Seeds contribute to adult replacement and to increases in local
population size and function as the means of dispersal to areas
distant from the local population (Louda 1982). Predation by
animals can be a key factor affecting seed mortality, with conse-
quences for plant abundance, distribution, and evolution (Duggan
1985; Harper et al. 1970; Moore 1978).
Seed predation can be grouped into predispersal and
postdispersal predation (Janzen 1971a), or pre-seedfall and post-
seedfall predation (Kjellsson 1985). Seed predators and dispersers
represent many species of animals including insects, birds, deer,
peccaries, squirrels, and mice. Among insects, Coleoptera, Hy-
menoptera, Diptera, Lepidoptera, and Thysanoptera constitute the
major seed predators. Diptera, Thysanoptera, Lepidoptera, and
some Coleoptera are predispersal predators; Coleoptera, Hy-
menoptera, birds, and some mammals are postdispersal predators.
Both larval and adult insects can function as seed predators. As an
example, both larvae and adults of the carabid beetle, Harpalus
rufipes, are seed predators in agroecosystems (Zhang 1993).
Predispersal predation by insects may cause mortality in up to 80%
of the seeds produced in many grassland and forest habitats
(Andersen 1988; Janzen 1971a, 1980), while postdispersal preda-
tion is often a major determinant of seed survival, plant species
distribution patterns, and plant community composition (Ashton
1979; Janzen 1972; Schupp 1988; Wilson and Janzen 1972). Table
1 lists insect seed predator species reported in the literature.

PREDISPERSAL SEED PREDATION

Predispersal seed predation refers to seed attack before the
seeds are shed by the parent plant. This type of seed predation by
insects is a widespread, often severe source of plant mortality
(Bohart and Koerber 1972; Harper 1977; Janzen 1969; Louda 1978;
Salisbury 1942). Examples of predispersal seed predation by in-
sects are compiled in Table 1. Many insect seed predators are
generalists, and therefore, the seeds of many plant species can be
attacked by a complex of taxonomically diverse insect species or a
mix of insect, bird, and mammal seed predators. A few plant species
appear to have only one species of predispersal seed predator
associated.
6 MAFES Technical Bulletin 163

Table 1. A list of insect seed predator species.

Order Family Species References

Coleoptera Bruchidae Acanthoscelides fraterculus* Green and Palmbald

1975
Bruchus atromarius* Crawley 1992
Mimosesta mimosae* Traveset 1990
Mimosesta nubigens* Traveset 1990
Sennius abbreviatus* Crawley 1992
Stator vachelliae Traveset 1990
Carabidae Amara sp. Imms 1948
Amara sp. Zhang 1993
Evarthus alternans Best and Beegle 1977
Evarthus sodalis sodalis Best and Beegle 1977
Harpalus fuliginosus Kjellsson 1985
Harpalus penslylanicus * Best and Beegle 1977;
Manley 1992
Harpalus rufipes Zhang 1994
Omophron sp. Imms 1948
Pterostichus chalcites Best and Beegle 1977
Pterositichus lucublandus Best and Beegle 1977
Zabrus sp. Imms 1948
Curculionidae Curculio glandium* Crawley 1992
Diethusa sp.* Auld 1986
Erytenna consputa* Neser and Kluge 1985
Melanterius sp.* Auld 1983
Melanterius acaciae* Auld and O’Connell
1989
Pseudanthonomus hamamelidis * DeSteven 1983
Pseudanthonomus virginiana* Crawley 1992
Rhinocyllus conicus Kok and Surles 1975
Rhyssomatus lineaticollis Franson and Willson
1983

Diptera Anthomyiidae Hylemya sp.* Hainsworth et al. 1984;

Crawley 1992
Pegohylemyia seneciella* Crawley 1992
Scatophagidae Gimnomera dorsata* Molau et al. 1989
Tephritidae Aethes deutschiana* Molau et al. 1989
Euaresta aequalis* Hare 1980
Neospilota signifera* Louda 1982
Orellia occidentalis* Lamp and McCarty
1982
Orellia ruficauda* Crawley 1992
Paracantha culta* Lamp and McCarty
1982
Trupanea wheeleri* Louda 1982
Urophora formosa* Louda 1982
Urophora sp.* Crawley 1992

Hemiptera Miridae Lygus boralis* Crawley 1992

MAFES Technical Bulletin 163 7

Table 1. continued.
Order Family Species References

Hymenoptera Eurytomidae Eurytoma sp.* Auld 1986

Formicidae Paratrechina vividula Alvarez-Buylla and
Martinez-Ramos 1990
Messor arenarius Abrahamson and Kraft
1965
Solenopsis geminata Risch and Carroll 1986

Lepidoptera Arctiidae Tyria jacobaeae* Crawley and Gillman

1989
Carposinidae Carposina autologa Neser and Kluge 1985
Cochylidae unidentified sp.* Louda 1982
Coleophoridae Coleophora alticolella* Randall 1986
Gelechiidae Sophronia sp.* Louda 1982
Geometridae Eupithecia cimicifugata* Willson 1983
Heliodinidae Heliodines nyctaginella* Kinsman et al. 1984
Incurvariidae Tegeticula sp.* Keeley et al. 1984
Noctuidae Dioryctyra sp.* Merkel 1967
Barbara sp.* Koerber 1962
Hadena sp.* Pettersson 1991
Oecophoridae Depressaria pastinacella* Sheppard 1987
Olethreutidae Laspeyresia sp.* DeSteven 1983; Kraft
1968; McLemore 1975;
Werner 1964
Pieridae Anthocharis cardamines* Duggan 1985
Pterophoridae unidentified sp. Louda 1982
Pyralidae Homeosoma electellum* Carlson 1967
Homeosoma stypticellum* Lamp and McCarty
1982
Tortricidae Clepsis peritana* Louda 1982
Phaneta imbridana Hare 1980
Epiblema scutulana* Leeuwen 1983
Cydia fagiglandana* Nielsen 1977; Nilsson
and Wastljung 1987
Phaneta imbridiana* Hare 1980

Orthoptera Gryllidae Hygronemobiu sp. Alvarez-Buylla and

Martinez-Ramos 1990
Thysanoptera Philoeothripidae Haplothrips sp.* Louda 1982
Thripidae Frankliniella minuta* Louda 1982
Frankliniella occidentialis* Louda 1982

* predispersal insect seed predator

8 MAFES Technical Bulletin 163

Predispersal seed predation of Cirsium arvense, Canada thistle,

by Orellia ruficauda (Diptera: Tephritidae) occurs in 20% to 85% of
the seed heads, and the proportion of damaged seeds per attacked
head averages 20%–80%, depending on geographical location and
sampling date (Forsythe and Watson 1985). Although the impact of
this seed predator is not severe enough to result in elimination of
this plant from an area where it is common, it is suspected to be an
important factor in the population regulation of C. arvense (Forsythe
and Watson 1985).
Quite often a complex of predispersal seed predators attack
plants. Kjellsson (1985) found two species of mice in the
myrmecochorous Carex pilulifera (Cyperaceae) (plants, dispersed
by ants) fields before seed fall. During the night, the mice climb the
Carex tufts, sometimes rising and reaching out for fruiting spikes.
Normally, the culm is bitten just below the spikes, resulting in an
oblique cut similar to cuts seen on damaged culms in the field.
These mice consume diaspores from 20 to 25 culms over two hours.
In addition to seed reduction from the mice, the ant species
Solenopsis flavicollis is a major harvester of C. pilulifera seeds
(Kjellsson 1985). It is estimated that S. flavicollis can reduce the
seed pool by 21.3%.
A northern Swedish population of Bartsia alpina, an arctic
perennial herb, is found to suffer high levels (normally 40%–50% of
the fruits) of predispersal seed reduction from the combined preda-
tion by larvae of two insect species: Aethes deutschinana (Lepi-
doptera: Tortricidae) and Gimnomera dorsata (Diptera:
Scatophagidae), both common seed predators of rhinanthoid
Scrophulariaceae plants (Molau et al. 1989). The level of tortricid
attack is more or less constant between years, and B. alpina seems
to be the primary host plant for A. deutschiana. The scatophagid
attack is lower than the tortricid attack, but more variable between
years. This is probably due to the fact that this predator has another
plant species, Pedicularis lapponica, as its main host. Also, the
degree of its attack on B. alpina depends on the ability of P.
lapponica to escape in time by shedding its seeds before adult
emergence of this scatophagid (Molau et al. 1989).
The intensity of predispersal seed predation by insects varies
with plant individuals. Traveset (1990) investigated two bruchid
beetles preying on seed of Acacia farnesiana. She found that the
intensity of seed predation varies notably among shrubs, without
showing any seasonal pattern. Assuming that adult bruchids move
among shrubs and that they can live up to three months and have
MAFES Technical Bulletin 163 9

several generations within the five- to six-month fruiting season,

an increase in seed predation might be expected during this period.
Predispersal seed predation by insects can be a key factor
determining the distribution of plant populations. Louda (1982)
investigated the variation in temperate shrubs Haplopappus
squarrosus and H. venetus over an elevational gradient in the
coastal sage scrub vegetation of San Diego County, California.
Haplopappus squarrosus and H. venetus are characteristic of
California coastal shrubs, the densities being higher on the coast
than inland (Louda 1982; Louda et al. 1989). In San Diego County,
they replace each other along an 80 to 100 km gradient from the
coast to inland mountains; H. squarrosus is found inland, whereas,
H. venetus predominates in coastal areas. Experimental exclusion
of seed predators at sites along a gradient from the coast to inland
mountains demonstrates two phenomena related to seed preda-
tion. First, predispersal seed predation limits seed input to the soil
and subsequently affects local seedling recruitment for both spe-
cies. Second, the net effect of these losses on adult plant distribu-
tion along the gradient changes as the physical conditions and
impact of other predators varies. For the inland species, H.
squarrosus, predispersal seed predation is the most important
factor explaining both local recruitment and reproductive age class
plant distribution over the gradient. Seedling recruitment is pro-
portional to the number of uneaten seeds; predation lowers seed
release differentially and is most severe at the coast. For control
plants (with seed predators, without pesticides), the distributions
of both seedlings and prereproductive age class plants exhibited the
same trend as the observed reproductive plant distribution. But,
for plants with seed predators excluded (with pesticides), the
distributions of both seedlings and prereproductive age class plants
corresponded to the reproductive age class plant distribution along
the gradient. Louda (1978) concluded that with H. squarrosus,
predispersal predators limit local recruitment and confine plant
abundance to the inland portion of its potential niche. For the
coastal H. venetus, seed predators also restrict seedling establish-
ment. In addition, seedling mortality, caused primarily by herbi-
vores and not by seed predators, is disproportionately severe
inland. Together, higher seed losses and higher seedling mortality
in the inland area restricted the observed distribution of H. venetus
to the coastal portion of its potential range (Louda 1978).
10 MAFES Technical Bulletin 163

POSTDISPERSAL SEED PREDATION

After seed has been shed from the parent plant it is available as
food for a wide variety of animals including small mammals, birds,
and insects. Postdispersal seed predation can occur on the soil
surface, in the soil, or on some other substrate. Traveset (1990)
found that the bruchid beetle, Stator vachelliae, finds seeds of the
leguminous Acacia farnesiana in the feces of horse, deer, and
ctenosaur lizards, the major Acacia seed dispersers in Costa Rica.
Bruchids attack a greater proportion of seeds at 1 m than 5 m from
the edge of a shrub’s crown (Traveset 1990). Female bruchids lay
eggs in seeds found on the surface of dung balls. The eggs hatch
and larvae eat the seeds. Female bruchids have a preference for
some seeds over others, and the attack rate varies in time and
space. The proportion of seeds attacked is not related to their
density in a dung ball.
As with predispersal seed predation, postdispersal seed preda-
tion can account for significant natural mortality. For instance,
Kjellsson (1985) found that the post-seedfall predation rate of
Carex piluifera in summer and autumn was 55% of the total seed
population in northeastern Zealand, Denmark (Kjellsson 1985).
Considerable seed mortality due to predation also occurred in the
spring. The Carex seed pool was reduced 86% by seed predation
(including pre-seedfall predation by mice). Mice and ground beetles
reduced the seed pool by approximately 21% and 65%, respectively.
Seed predation ranging between 30% and 80%, has been reported
for several woodland myrmecochores (Culver and Beattie 1978;
Heithaus 1981).
Though insects are known to be important postdispersal seed
predators in most terrestrial forests, they also play an important
role in marine tidal (mangrove) forests. A survey at 12 sites along
the tropical Australian coast showed that between 3.1% and 92.7%
of the seeds or propagules of 12 mangrove tree species were
attacked by insects (Robertson et al. 1990).
Carabid beetles, ants, and rodents are the most studied
postdispersal seed predators. More research has been conducted on
ants and rodents as seed predators than on carabids. Predation
behavior differs greatly between rodents and ants. A study con-
ducted in the Israeli desert (Abramsky 1983) indicates that preda-
tion behaviors were similar to those reported for the same two
groups in deserts of North America (Mares and Rosenzweig 1978).
Rodents find seeds under the soil surface by olfaction, and are more
efficient than ants at finding and harvesting seeds. In contrast,
MAFES Technical Bulletin 163 11

ants can not find seeds under the soil surface. A second difference
relates to the timing of predation behavior: rodents are nocturnal,
while ants are mostly diurnal. Large seeds are utilized first by
rodents, a shift to small seeds occurs only after most of the large
seeds have been utilized. Rodents are primarily seed predators,
while ants act also as seed dispersers. The interference of ant
predation from rodent predation is minimal as ants continue their
foraging even while seeds in trays are replaced (Abramsky 1983).
Competition may occur between ants and rodents for seeds in low
density Acacia stands (Holmes 1990).
Ants show an interesting seed preference behavior. Risch and
Carroll (1986) found that in feeding preference field studies, the
amount of each seed type removed by ants was strongly influenced
by the amount and kinds of other seeds in the immediate area. A
strongly preferred seed is removed less frequently if it occurs in the
midst of non-preferred seeds. Non-preferred seeds are taken much
more readily if they occur with preferred seeds (Risch and Carroll
1986). Studies allowing ants free passage to seeds, but excluding
larger seed predators show that seed predation of the tropical
pioneer tree, Cecropia obtusifolia, was not significantly different
from uncovered control seeds, indicating that ants were the pri-
mary seed predators. The distribution of seed predation rate by
ants after four days of experimentation was bimodal, suggesting
once ants discover a dish of seeds, all of them are taken (Alvarez-
Buylla and Martinez-Ramos 1990).
Seed predation by the Carabidae was reported as early as the
1880s (Forbes 1880, 1883; Johnson and Cameron 1969; Webster
1880, 1900). Nitzsche (1893) reported that carabid beetles of the
genus Harpalus destroyed up to 80% of the seed and seedlings in
nursery beds. Predation rate by carabids varies with predator and
prey species. Lund and Turpin (1977) tested predation by five
Carabidae species on six seed species. In a test to determine if
beetles would attack weed seeds in the laboratory, Harpalus
pensylvanicus damaged more seeds than other carabid species.
However, the number of seeds damaged varied with the seed
species. Pterostichus chalcites and P. lucublandus damaged simi-
lar numbers and species of seeds, but only chickweed, Stellaria
media, was damaged in high numbers. The carabid Evarthrus
sodalis sodalis damaged only a few seeds of any species (Lund and
Turpin 1977).
Further study of predation by Harpalus pensylvanicus showed
that predation rate varies with seed species. On the basis of
predation preference over a 40- hour period, seed species could be
12 MAFES Technical Bulletin 163

grouped into three to five categories (Lund and Turpin 1977). Best
and Beegle (1977) found that H. pensylvanicus and Evarthrus
alternates feed on many kinds of seeds with preference for smooth
dock seeds, barnyard grass seeds, and yellow foxtail seeds. Lund
and Turpin (1977) found that H. pensylvanicus prefers green
foxtail, Setaria viridis var. major, over other seed species tested.
The size of seeds tested might influence the number of seeds
damaged in one of two ways. Larger seeds provide more food per
seed, and it requires fewer seeds to satiate the animal. Also, the size
and shape of the seed might affect the ease with which the beetle
can handle and open the seed. Preference for one seed species over
another might well be due to the ease of handling and opening of the
seed rather than selection based on textural or chemical clues
(Lund and Turpin 1977).
Although H. pensylvanicus is usually a postdispersal seed
predator (Best and Beegle 1977; Lund and Turpin 1977), it may also
act as a predispersal seed predator in specific habitats. Manley
(1992) found that H. pensylvanicus adults have more impact on
seed production prior to seed maturity than afterwards. Beetle
populations in 1992 were highest prior to seed maturity. Caged
adults fed on both individual mature seeds of grasses and develop-
ing seed heads. Adults readily fed on inflorescences of crabgrass
and fall panicum (whose heads are near or on the soil surface), but
not on green foxtail (whose seed heads are distant from the soil
surface), though beetles fed on individual green foxtail seeds. This
suggests that H. pensylvanicus may readily attack immature seeds
or seed heads when they are near the soil surface.
Considerable research has been conducted on the postdispersal
seed predation of the European carabid Harpalus rufipes. This
species is primarily a seed predator (Briggs 1965; Curtis 1860;
Forbes 1880, 1883; Johnson and Cameron 1969; Luff 1980; Skuhravy
1959; Webster 1880, 1900; Zhang 1993; Zhang et al. 1994; Znamenskii
1926); however, when seeds are in low relative abundance, H.
rufipes will feed on small insects (Chiverton 1987; Coaker and
Wiliams 1963; Cornic 1973; Dempster 1967; Hamon et al. 1990;
Rivard 1966; Sunderland 1975; Sunderland et al. 1987; Zhang et al.
1994). Adults have been observed to feed on the seeds of 29 of 38
species of plants in the laboratory (Briggs 1965; Zhang 1993).
Preference for seed species is shown by H. rufipes adults (Zhang
1993). Grasses are a preferred type of seed along with small seeds
such as common lambsquarters, Chenopodium album, and dande-
lion, Taraxacum officinale. Seeds of species in the Cruciferae are
the least preferred. The mode of feeding is associated with seed
MAFES Technical Bulletin 163 13

species as is the functional response (Zhang 1993). Adults exhibit

a type II functional response (Price 1984) to preferred seeds and a
type I response to less preferred seeds.
Larvae of H. rufipes are also seed predators. Larvae scrape soil
away from the terminal cell of the tunnel with their mandibles and
press it into the side of the burrow with the dorsal surface of the
head. Seeds are carried in the mandibles before being embedded in
the side of the burrow with the head. There is often a closely packed
cache of seeds just above the terminal cell where the larvae
consume single seeds (Thiele 1977). Luff (1980) found that second
instar larvae of H. rufipes fed on 18 out of 24 species of seeds offered
in a choice test. Eight “favorable” species were eaten by at least six
of ten larvae to which they were offered. These species were Lolium
perenne, Festuca rubra, Chenopodium album, Agrostis tenuis,
Dactylis glomerata, Trifolium repens, Senecio jacobaea , and
Medicago lupulina. The remaining “unfavorable” species were
Brassica rapa, Cardamine amara, Scabiosa columbaria, Brassica
oleracea, Hypericum perforatum, Antennaria dioica, Campanula
rotundifolia, Heracleum sphondylium, Sisymbrium officinale, Bras-
sica napus , Filipendula ulmaria, Geum urbanun , Hesperis
matronalis, Scutellaria galericulata, and Solanum dulcamara.
When given a choice among six “favorable” seeds offered two at a
time, the ranking was similar to that when the same seeds were
offered without choice, although a more distinct division appeared
between grasses and C. album, which were highly preferred, and
the remaining two lesser preferred seed species.
Germinating seeds are also damaged by H. rufipes. Larvae feed
on the endosperm of germinating seeds of perennial rye grass
(Loliu perenne). The larval growth rate is more rapid with germi-
nating seeds of lambsquarters, C. album, groundsel, Senecio vul-
garis, and the grasses Agrostis tenuis, Festuca ovina, and Phleum
pratense, than with those of perennial rye grass and cereals. There
are no differences between the feeding rate on germinating and
non-germinating seeds of L. perenne. The mean numbers of germi-
nating and non-germinating seeds eaten by ten larvae were 2.8 ±
0.4 and 2.8 ± 0.3, respectively (Luff 1980).
H. rufipes is associated with cultivated habitats and is most
abundant in small fields as compared to large agricultural fields
(Traveset 1991). Another characteristic of fields that may affect H.
rufipes abundance is “weediness.” Speight and Lawton (1976) used
an artificial prey to test the effect of the weed Poa annua in cereal
fields on the abundance of carabids, including H. rufipes. Within
one field, areas of high weed cover had more predatory ground
14 MAFES Technical Bulletin 163

beetles, and artificial prey suffered significantly greater ‘mortality’

than areas with few weeds. Diversity of weed species has been
suggested to be important for ground beetle populations (Murdoch
et al. 1972; Pimental 1961; Speight and Lawton 1976). The relation-
ship between beetle activity and the frequency and abundance of
Poa annua is probably complex, but it is likely that the role that the
weeds play in protecting the predators from weather extremes, i.e.,
insolation during the day, and desiccation, both during the day and
at night, is important (Speight and Lawton 1976). Rivard (1966)
found higher catches of carabids in areas of higher humidity, and
Thiele (1964) considers that relative humidity is a key factor in the
abundance of the majority of carabids and that microclimate in
vegetation is very important. High weed densities provide a high
relative humidity. It is also possible that there is an indirect effect
of weed density due to the abundance of natural prey, which may
be more common in dense weed patches (Speight and Lawton 1976).
However, exception to the weediness hypothesis exists. Purvis and
Curry (1984) found that none of the dominant carabids they studied
respond positively to weediness. Although, the activity of P.
melanarius appeared to persist longer in weedy plots in September,
both this species and H. rufipes were equally active in all plots
during their peak abundance in August. One possible reason may
be the crop (beet) provides shade and high relative humidity even
in the absence of weeds.
Cultivation may favor H. rufipes because of larval require-
ments for seeds as food. An open soil surface encourages weed
growth, and H. rufipes larvae would be short of food in a field kept
completely weed free (Luff 1980). After using pitfall traps to
investigate the carabid fauna of arable land, Scherney (1960)
concluded that certain Carabidae (H. rufipes included) were asso-
ciated with cultivation; the numbers taken in pitfall traps in
different habitats were in the following order: wheat fields > barely
> potato > clover > grass meadow > densely weed-covered waste
ground. Although agricultural monocultures are considered un-
stable habitats, they may provide stable conditions for species
dependent on relatively bare, loose cultivated soil, such as H.
rufipes (Luff 1980).
Other environmental factors also have an impact on seed
predation rate by carabids. Brust and House (1987) investigated
weed seed loss in conventional till and no-till soybean
agroecosystems. Seeds of four broadleaf weed species (ragweed,
pigweed, sicklepod, and jimson weed) and one grain crop species
(wheat) were provided in a free choice design with densities of 10,
MAFES Technical Bulletin 163 15

25, and 50 seeds per 24 cm3 of soil. Approximately 2.3 times more
seeds overall, and 1.4 times more large seeds as a group were
consumed in no tillage systems than in conventional tillage systems.
In low-input, no-tillage treatments, large ground beetles (15–
25 mm) and mice preferentially fed on the large seed species, while
small carabids (< 15 mm), ants and crickets, fed almost exclusively
on the smaller seed species. Carabid beetles were responsible for
more than half of all seeds consumed (Brust and House 1987). The
difference in predation rates between no-tillage and conventional
tillage systems can be explained by the differences of the seed
predator abundance as a result of soil disturbance. In the south-
eastern United States, conventional tillage systems (moldboard
plow/disk) generally support fewer soil arthropods than no-tillage
systems (Blumburg and Crossley 1983; House and All 1981; House
and Parmelee 1985). Soil disturbances in natural ecosystems can
also depress soil arthropod numbers, resulting in a concomitant
reduction in seed predation (Mittelbach and Gross 1984).

SEED PREDATION AND PLANT POPULATION

DYNAMICS
Plant Population Recruitment
Seed predation may influence plants at both the population and
individual levels. At the population level, potential effects include
(a) lower recruitment rate due to reduction in occupancy of “safe
sites” (Louda 1978) suitable for germination and establishment, (b)
discontinuous recruitment due to periodic or “mast” fruiting and
the accompanying satiation of seed predators (Janzen 1971a), and
(c) alternation of adult distribution, due to density dependent seed
predation (Janzen 1971a). The potential consequences of seed
predation at the individual level have been less widely explored.
Seed production and spatial location may influence the severity of
predispersal predation on different individuals (Moore 1978). The
ecological result is that the relative contribution of some adults to
successful seed production will be greater than that of others, and
may be so consistently, from year to year. If these traits are heritable,
the evolutionary result is a selective force upon adult characteristics
that confers relative escape from predation (DeSteven 1983).
Evaluation of predation in seed bank dynamics is either trivial
or surprisingly difficult. Seed consumption is a major gustatory
strategy that causes significant seed losses. So in the trivial sense,
seed predation, like any mortality factor causing a consistent loss
of young, will influence population ecology and evolution. Consis-
16 MAFES Technical Bulletin 163

tent losses have a potential impact on plant abundance, distribu-

tion, competitive status, life cycle traits, and other adaptations.
Differences in damage among individuals or between species can be
significant even where the magnitude of the loss is small.
Seed predation rate may be related to seed size. Reader (1993)
found adding a cage to reduce seed predation, especially by ants,
did not increase seedling emergence significantly for small seeds
(0.06–0.14 mg). In contrast, seedling emergence increased signifi-
cantly for larger seeds (0.15–12.2 mg) (Reader 1993). Seed preda-
tion not only affects the number of seeds, but also reduces the seed
viability. Andersen (1988) compared two methods of studying
insect predation on seeds in Australia. The conventional method
(inspecting insect attack symptoms) indicated that insects at-
tacked only 2%, 10%, 28%, and 1% respectively of Eucalyptus
baxteri, Leptospermum myrsinoides, L. juniperinum, and Casua-
rina pusilla seeds, whereas bagging experiments indicated that
insects reduced seed production by 66%, 64%, 44%, and 83%,
respectively. Therefore, if the bagging experiments reflect a more
accurate picture of predation, then insect seed predators may cause
far greater losses than they appear to (Andersen 1988).
How important is seed predation to recruitment in stable
populations of long-lived perennials? The importance of seed losses
to population recruitment at any point in time is related to the
abundance of “safe sites.” Insect seed predation rate can be very
high, up to 100% of the seed population (Sallabanks and Courtney
1992). However, these losses do not necessarily have an important
impact on population recruitment because (a) in most years preda-
tion is not 100%, (b) in most years recruitment appears to be limited
by a rarity of safe sites and not by seed supply, and (c) the losses do
not prevent the establishment of large seed banks (ranging from 30
to 1,100 viable seeds per m2) potentially capable of exploiting
temporary conditions favorable for recruitment (Sallabanks and
Courtney 1992).
Seed-feeding insects, as compared with leaf-feeding ones, often
destroy a large fraction of their food supply (Janzen 1971a).
Although seed predation rate may be high on the average, it is also
highly variable (House and Parmelee 1981). The dynamics of a
seed-predator system seems to depend primarily on how seed
predator populations “track” their variable resources in time and
space (Solbreck and Sillen-Tullberg 1986). At present, few seed
predation models are available. Reduction of the seed bank through
seed predation can be expressed as an exponential decay curve
(Boucher 1981):
MAFES Technical Bulletin 163 17

dN / dt = -kN;
where N is the seed number in the seed bank, t is time, and k the
constant instantaneous removal rate. The number of seeds in the
seed bank at any time (t) is
Nt = N0 exp -kt
This relationship may be affected by seed size. Removal rate may
decrease with increasing seed size and there maybe a satiation
effect (Boucher 1981).

Seed Dispersal
Seed removal has two effects on the seed bank. At high plant
densities, seeds can be removed and eaten by all seed-predating
and dispersing animals. Therefore, high densities of the seed
predators and dispersers will play an important role in reducing
the seed bank. At low plant densities, there will be competition
between seed predators and seed dispersers. Seed predators such
as rodents consume seed where it is found and directly reduce the
seed bank. Whereas, a high population of ants (dispersers) will
remove seeds from the surface to other locations, where seeds may
accumulate for the next generation. At this point, seed dispersers
are beneficial to the recruitment of the next plant generation.
Holmes (1990) demonstrated this interaction while investigating
seed removal in the litter layer of Acacia spp. stands at bimonthly
intervals throughout a one-year period. He found that both ants
(dispersers) and rodents (predators) removed significant quantities
of seeds and may compete for seeds in low density stands. Seed
removal from artificial depots by invertebrates was greatest prior
to seed-fall (September–November) and lowest during seed-fall
(January–March). Rodents may consume a large proportion of the
annual seed production at low Acacia spp. densities, but ants play
a critical role in accumulating seed banks.

Spatial Patterns of Plants

Seed predation rates may also determine plant spatial pat-
terns. In two experiments, Alvarez-Buylla and Martinez-Ramos
(1990) found that ants (Paratrechina vividula) and grasshopper
nymphs (Hygronemobius spp.) were the dominant seed predators
of the tropical pioneer tree, Cecropia obtusifolia. Removal rates
ranged from 27% to 98% in four days and were significantly higher
in gap and mature patches than in building patches. Together with
pathogens, predators resulted in low survivorship of the tropical
18 MAFES Technical Bulletin 163

pioneer tree seeds and a rapid turnover rate of its seed bank (1.02
to 1.07 years) (Alvarez-Buylla and Martinez-Ramos 1990).
Whelan et al. (1990) examined the spatial and temporal pat-
terns of postdispersal seed predation of vertebrate-dispersed plant
species (Cornus drummondii and Prunus americana) in temperate
woodland and old-field habitats. Rates of seed loss by all predators
including insects varied with microhabitat (near logs, tree trunks,
and open forest floor), macrohabitat (old-field, forest), plant spe-
cies, year, and time of dispersal within a year. The levels of final
mortality of seeds did not vary with microhabitat or time of dispersal,
but did vary between macrohabitats, plant species, and years.
As discussed previously, a study conducted by Louda (1978)
showed that the plant H. squarrosus is confined to inland portions
of its potential niche due to the seed predation of insects. In turn,
the distribution of seed resources may affect seed predation. Seed
predation in relation to patterns of pod (and seed) distribution was
examined in five samples of the common milkweed ( Asclepias
syriaca), in tests of the “resource-concentration” effect both within
and between plants (Franson and Willson 1983). Plants with large
clusters of pods produced more undamaged pods, and, by this
measure, were more successful than plants with small clusters.

Adaptation
Theoretically, seed predation, like other forms of predation,
should cause two types of response by the exploited plant popula-
tion. The first is adaptation, via selection for morphological, chemi-
cal, temporal, and spatial mechanisms of predator avoidance. The
second is modification of numerical and spatial occurrence, via
elimination and redistribution of better-adapted individuals in the
population through differential patterns of attack (Harper 1969;
Janzen 1969, 1971a, 1971b; Louda 1978). Although variability in
the damage to seeds is generally high, seed predation is thought to
represent a strong selective force acting on protective structures
(Janzen 1969, 1970; Smith 1975); dispersal phenology (Heithaus
1981; Janzen 1971b; Silvertown 1980); and dispersal method (Beattie
and Lyons 1975; O’Dowd and Hay 1980). The dispersal of seeds
from the parent plant and its surroundings is often thought to
decrease the risk of predation and pathogen attack (Augspurger
1983; Harper 1977; Janzen 1969; Wilson and Janzen 1972). Hence,
it has been suggested for several genera (e.g., Viola, Sanguinaria,
Asarum) that seed predation has been an important selective force
in the evolution of myrmecochory (Beattie 1983, Beattie and Lyons
1975, Heithaus 1981, O’Dowd and Hay 1980).
MAFES Technical Bulletin 163 19

Seed predation may also be a selective factor influencing the

evolution of seed protective characteristics such as spine length
and wall thickness of burrs. In a study of Xanthium strumarium,
predation was found to be more intense in populations with low
mean burr length and to decline linearly with increasing burr
length (Hare 1980). Ten populations of X. strumarium occurred in
quite similar habitats in proximity to each other, but showed quite
striking differences in burr size and susceptibility to seed preda-
tors. Mean burr length varied between 15.4 and 19.5 mm among
populations, and the percentage of attacked burrs varied from 3%
to 84% among populations in one year. Burr length variation
among populations is primarly genetically controlled, and differ-
ences in susceptibility among populations persisted when plants
were grown under uniform conditions and uniformly exposed to
insect attack. The probability of attack declined linearly with
increasing burr length under both field and experimental condi-
tions. Susceptibility was negatively correlated with mean burr
length among plants when plants from all populations were pooled.
Seed predation was also higher in populations with a lower mean
burr length. Thus, by attacking smaller burrs, Hare (1980) sug-
gests that these insects can be important natural selection agents
for increased burr size. On the basis of oviposition behavior of the
two insects, Euaresta aequalis (Diptera: Tephritidae) and Phaneta
imbridana (Lepidoptera: Tortricidae), thicker burr walls and longer
burr spines could reduce the insects’ ability to penetrate burrs.
These characteristics were positively correlated with burr length,
thus shorter burrs may be more successfully attacked because they
are more easily penetrated (Hare 1980).
Seed predation and the coexistence of tree species in tropical
forests were studied by Hubbell (1980). Host-specific seed and
seedling predation can explain the coexistence of the large number
of tree species in tropical forests (Harper 1977). Janzen (1970)
noticed that virtually all seeds underneath the parent are killed by
seed predators, and proposed that only those viable seeds that are
transported some distance from the parent have any significant
chance to escape discovery and germinate. Accordingly, such
predation should lead to a low density of, and wide spacing
between, adult trees. This would prevent any one species from
becoming dominant, provided those seed sources for other species
exist to fill the available habitat (Janzen 1970). Connell (1971)
argued that predation was a much more likely agent than interspe-
cific competition to prevent single-species dominance in tropical
forests. In optimal climates, predator abundance should build until
20 MAFES Technical Bulletin 163

they are resource limited. He postulated that host-specific herbi-

vores (principally folivores) attracted by adult trees would also
discover, defoliate, and kill all seedlings in the vicinity of adult
trees. Seedlings are presumably less resistant to defoliation. Again,
habitat in the neighborhood of adults of one tree species would be
open for colonization by juveniles of other tree species, and diver-
sity would be maintained. Seed density and the probability of seed
survival can be expected to change with increasing distance from
the parent tree because fewer seeds are expected to be carried to
greater distances from the parent (Connell 1971). Regardless of the
mode of seed dispersal, the “seed shadow” (seeds per unit area)
curve is a monotonically decreasing function of distance from the
parent tree (Willson 1992). On the other hand, because seed and
seedling predation are greater near the parent, the per capita
chance of seed survival to maturity is a monotonically increasing
function of distance from the parent. The product of the seed
shadow and the per capita chance of seed survival to maturity
curves describes the density of offspring that survive to maturity at
different distances from the parent tree (Hubbell 1980).
Temporal patterns of plant reproduction may also be a result of
seed predation. “Mast seeding” or “mast fruiting” describes the
phenomenon of synchronous production of seeds within a plant
population in one year followed by an interval when few seeds are
set. This is a widespread phenomenon among temperate floras and
is common in hardwood trees and conifers (Harper 1977). Seed
predators can act as a selective force favoring mast fruiting, due to
the excessive seed losses incurred by the asynchronous individuals
that fruit in “off-peak” years. High predispersal seed predation in
poor fruiting years might also enhance fruiting periodicity, if, by
preventing seeds from maturing, the resources that would have
been used for maturation are instead stored for use in a subsequent
year. The weevil Pseudanthonomus hamamelidis is host specific
and univoltine on witch hazel (Hamamelis virginiana). The fluctu-
ating pattern of fruit production is a key feature in understanding
the demographic impact of seed predation on witch hazel (DeSteven
1983). DeSteven (1983) observed that fruit production fluctuated
between 1977 and 1980. In poor fruiting years (1977 and 1978),
oviposition sites were limited due to low fruit abundance and attack
percentages on fruit crops were high. The size of the weevil
population appeared to be resource limited in such years, since
searching weevils may be unable to find particular individual
plants because they are small, have very few fruits, or are ex-
tremely isolated from conspecifics. Following poor fruiting years,
MAFES Technical Bulletin 163 21

the fruit crop in a production year “satiates” the relatively small

weevil population, with the result that seed predation intensities
are substantially lower, and more seeds escape predation. Contin-
ued high fruit production allows an annual increase in weevil
numbers and in fruit attack; however, any reduction in fruit
production following a good fruiting year lowers weevil population
size, and fruit attack increases. The result for witch hazel is a pulse of
successful seed survival in the occasional production year that satiates
the seed predator population (DeSteven 1983). Similar patterns of
high seed predation in years of poor seed production have been
observed in a number of forest trees, where fluctuating fruiting
patterns also appear to regulate seed predator populations (Abrahamson
and Kraft 1965; Gardner 1977; Mattson 1971; Miller 1973).
Ballardie and Whelan (1986) investigated the relationship
between masting and seed dispersal, and seed predation in the
cycad Macrozamia communis and found that the result was differ-
ent from DeSteven’s (1983) study. They found that dispersal of
seeds by opossums was poorer from source plants in a masting
population than from source plants in an adjacent, non-masting
population (Ballardie and Whelan 1986). This resulted in fewer
seeds per seeding female plant in the masting plot being dispersed
to favorable sites. Predation of seeds over the year of the experi-
ment was much more severe in the masting plot than in the
nonmasting plot. Very few seeds were touched by rats in the non-
masting plot. Masting did not allow any escape from predation. The
absolute number of seeds eaten in the masting plot was more than
ten times greater than in the nonmasting plot. They suggest that
the mast seeding observed in M. communis may not be adaptive,
but is more likely a consequence of other factors, which synchronize
flowering within local populations (Ballardie and Whelan 1986).

Plant Community Dynamics

A few studies have shown that seed predation can affect plant
community structure. A native fire ant, Solenopsis germinata, was
observed to harvest small seeds, especially grasses, in disturbed
habitats in wet tropical areas of Mexico and Central America
(Inouye et al. 1980; Risch and Carroll 1986). If common, this ant can
lower overall abundance of many weedy species. When the ant
exhibited a strong preference for seeds from one plant species, total
plant biomass was significantly lower (by up to 50%) in plots with
ants for about the first 50 days after planting. Subsequently, the
non-preferred species increased, and 83 days after planting, total
plant biomass was about the same in the presence and absence of
22 MAFES Technical Bulletin 163

ants. Seeds of Paspalum distichum were highly preferred by the

ants, while Daucus carota were rejected. In the absence of ants, P.
distichum is competitively superior to D. carota. Ants reverse the
course of plant competition. Thus, P. distichum contributed little
to total weed biomass. A crop growing with ants can thus benefit
from reduced competition early in the season (Risch and Carroll
1986). Due to seed preference, ants may selectively remove domi-
nant small seeds, and as a result, increase the community diversity
and evenness (Inouye et al. 1980).

WEED CONTROL WITH SEED PREDATORS

Seed predation provides potential for classical biological con-
trol of weeds by seed predators (Julien 1982). Weevils have proven
to be good candidates in weed integrated pest management (IPM)
programs. Rhinocyllus conicus, a thistle-head-feeding weevil in-
troduced from France successfully controlled Carduus nutans
(musk thistle) at a Virginia release site (Pulaski County) six years
after the initial release of 100 adults in 1969. Thistle density was
reduced by 95%. In 1974 and 1975, about 90% of the thistles were
attacked by the weevil; more than 10% of the terminal heads were
aborted. Persistent pressure from increasing weevil population on
the thistles brought about dramatic changes in the thistle problem
(Kok and Surles 1975). Furthermore, 11 years of inter-species
population dynamics study at two release sites, Frederick County
and Pulaski County in Virginia, shows that thistle reduction was
dramatic after the explosive phase of the weevil build-up during the
fifth year after release. This was followed by weevil dispersal and
resurgence of plant density. However, the resurgent plants were
smaller and produced fewer buds than the thistles prior to weevil
release; thus bud density during resurgence was significantly
lower than the initial density. Between 1969 and 1980, decline in
musk thistle bud numbers was 80% at the Frederick County site
and 97% at the Pulaski County site (Kok and Pienkowski 1985). R.
conicus, when introduced into San Luis Obispo County, California,
also played an important role in the control of Italian thistle,
although the seed loss was only 55% (Goeden and Ricker 1985).
Neser and Kluge (1985) found an introduced seed predator to
show promise in weed control in South Africa. Hakea sericea
(Proteaceae), a fire-adapted woody plant from Australia, is an
important weed in the species-rich vegetation of the Cape Moun-
tains, South Africa. This weed occurred over nearly half a million
ha, mainly in mountainous areas in dense, impenetrable thickets.
MAFES Technical Bulletin 163 23

The seeds remain viable in woody follicles that accumulate on the

plant over the years. It was estimated that 75 million seeds/ha may
be accumulated on 15-year-old stands. From surveys of natural
enemies in Australia, two complementary seed-attacking species
were selected and tested for release in South Africa. These are the
weevil Erytenna consputa (Coleoptera: Curculionidae) whose lar-
vae develop in, and cause the death of, young fruits, and the moth
Carposina autologa (Lepidoptera: Carposinidae) that develops on
seeds inside mature follicles accumulated on living plants. Erytenna
consputa is strikingly adapted to its host and to surviving fires. The
weevil was established in South Africa after the release of small
numbers of field-collected adults from different climatic regions in
Australia. Climatic matching was not as important as host strain
matching in the establishment of the weevil. Following establish-
ment, E. consputa has greatly (up to 86% of the total fruit
mortality) reduced seed accumulation by H. sericea and has started
to suppress the dense regeneration of the weed. However, addi-
tional agents may be required for an integrated control program
against this weed from Australia (Neser and Kluge 1985).
Other insect seed predators that may have potential for classi-
cal biological control are the seed beetle Spermophagus sericeus
(Bruchidae) for control of field bindweed, Convovulus arvensis
(Rosenthal 1985; Rosenthal and Buckingham 1982); the flower-
and seed-feeding weevil Acallopestus maculithorax for control of
velvetleaf, Abutilon theophrasti (Mittelbach and Gross 1984); and
two seed predatory weevils, Ceutorhynchus turbatus and C.
parvilus, for control of hoarycress, Cardaria draba (Lipa 1974).
Inundative release strategies for temporary (one to five years)
reduction of weed seed banks has not become a tactic in IPM
programs. This is probably due to the expense and difficulty in
rearing the necessary numbers of seed predators for such a man-
agement tactic relative to the cost of herbicides (Deloach 1978).
A promising tactic for weed management that has also not been
implemented is conservation of existing weed seed predators
(Liebman and Janke 1990). This tactic has advantages over classi-
cal biological control approaches, which rely on foreign introduc-
tions. Considerations such as attack of non-target host plants or
competitive exclusion of native insect species are usually not
significant concerns (Charudattan and Deloach 1988). Carabids
and ants are ideal candidates for conservation in north temperate
US agroecosystems (Best and Beegle 1977; Blumburg and Crossley
1983; Brust and House 1987; House and All 1981; House and
Parmelee 1985; Johnson and Cameron 1969; Lund and Turpin
24 MAFES Technical Bulletin 163

1977; Manley 1992; Mittelbach and Gross 1984; Reader 1993; Risch
and Carroll 1986; Rivard 1966; Webster 1880; Zhang 1993). Conser-
vation of these seed predators in agroecosystems requires that
their life systems be understood in sufficient detail so that IPM
programs can be designed that minimize mortality and maximize
seed predator population growth, under the constraints of manag-
ing insect pests in an agroecosystem (Bird et al 1990). The impact
of factors such as tillage (Brust and House 1987; House and
Parmelee 1985), cover crops (Reader 1993; Zhang 1993), rotation
crops (Zhang 1993), and pesticides (Zhang 1993) on the population
dynamics of weed seed predators must be investigated for each
insect species targeted for conservation. Landscape features such
as field borders, topography, and spatial pattern and aggregation
of farm lands and forests have not been studied in regards to the
population dynamics of insect seed predators. There have been
many field studies conducted that assess removal rates and mortal-
ity rates of seeds under field conditions, however, there is a general
dearth of information on the quantification of insect seed predator
numerical and functional responses and interference rates under
field conditions (Zhang 1993). The lack of manipulative field
studies of weed management by conservation of insect seed preda-
tors probably reflects the limited amount of research that has been
conducted in the area of alternatives to herbicide based weed
management (Liebman and Janke 1990).
We hope that this review has provided a framework for under-
standing the mechanisms of insect seed predation, the diversity of
insects that prey on seeds, and the ecological and evolutionary
consequences of insect seed predation. Insect seed predation can
play significant roles in reducing plant population growth, modify-
ing intraspecific and interspecific competition, shifting spatial and
temporal distribution, affecting species evolution, and plant com-
munity structure, both in natural and agricultural ecosystems.
Further study on insect seed predation-plant population dynamics,
insect seed predator behavior, and how to economically incorporate
insect seed predators into integrated weed management programs
are all important areas of investigation with regards to insect
predation of seeds. We have found, by reviewing the literature, that
there is a lack of research that attempts to link weed or plant
population or community dynamics with the population or commu-
nity dynamics of insect seed predators. Most studies focus solely on
either the plant’s population dynamics or the insect seed predator’s
population dynamics. The challenge, therefore, in the future is to
develop a theoretical basis for the ecology of seed predation.
MAFES Technical Bulletin 163 25

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